Skip to main content
Asian Journal of Neurosurgery logoLink to Asian Journal of Neurosurgery
. 2019 Apr-Jun;14(2):422–426. doi: 10.4103/ajns.AJNS_161_18

Small Aneurysms Should Be Clipped?

Gustavo Noleto 1, Nícollas Nunes Rabelo 1, Leonardo Abaurre 1, Hugo Sterman Neto 1, Mario Siqueira 1, Manoel J Teixeira 1, Eberval Gadelha Figueiredo 1,
PMCID: PMC6516009  PMID: 31143256

Abstract

Background:

Cerebral aneurysm prevalence may vary from 0.4% to 10%. The decision to treat or not incidental aneurysms remains controversial, especially when the lesions are small (<5 mm). Many recent publications are demonstrating that these lesions often bleed.

Methods:

We reviewed admitted patients with angiographic studies submitted to intracranial aneurysm surgical treatment from April 2012 to July 2013 in the Neurosurgery Department of São Paulo Medical School University (15 months), to define the rate and risk of bleeding. In addition, we proceeded literature review with collected 357 papers (past 5 years) which were selected 50 that were focused on our research. Clinical patients’ status at the time of discharge was evaluated with the modified Rankin scale.

Results:

A series of 118 cases of surgically clipped aneurysms was analyzed: 73.7% woman; Ruptured (61 cases, 51%); middle cerebral artery (51 cases, 43%) was the more common aneurysm. Small size (<5 mm) was 25 cases (21%); that 2 died (16%), 3 (25%) with severe disability,restricted to bed and dependent on nursing care; blood pressure was the main risk factors (56%); and an aneurysm <2 mm (100%) was ruptured.

Conclusion:

The number of small aneurysms in our series was significant (25 cases, 21%), and its rate of bleeding was high (25 cases, 48%), resulting in death and disability in a significant number of cases. Our tendency is for surgical treatment when it is associated with risk factors.

Keywords: Aneurysm clipped, cerebral hemorrhage, intracranial aneurysm, small cerebral aneurysm, subarachnoid hemorrhage

Introduction

Cerebral aneurysm prevalence may vary from 0.4% to 10%.[1,2] The incidence of subarachnoid hemorrhage (SAH) ranges from 6 to 21.6 per 100,000 persons per year, depending on the study population and methodology.[2,3,4] A more significant number of related cases have been identified with the development and availability of more sophisticated brain diagnostic methods. Despite this, the management of these aneurysm groups is still controversial. There is no consensus about the best treatment for an incidental aneurysm, especially when it is small.

According to the International Study of Unruptured Intracranial Aneurysms, the risk of rupture of anterior circulation aneurysms smaller than 7 mm is only 0.1% per year. However, experienced neurosurgeons and interventional neuroradiologists reported that, in clinical practice, small aneurysms are ruptured in most of the time,[5,6,7,8] and the SAH after small aneurysm rupture is often more significant, compared to massive aneurysm rupture.[8,9]

In this paper, the authors present one series analysis of small ruptured and intact aneurysms, treated surgically in the past 15 months, emphasizing clinical and surgical aspects of aneurysms smaller than 5 mm.

Methods

We reviewed the electronic files and admitted patients with angiographic studies submitted to intracranial aneurysm surgical treatment from April 2012 to July 2013 in the Neurosurgery Department of São Paulo Medical School University. This study was approval in our Institutional Board Review.

Patients were characterized by age and gender. The aneurysm localization, the occurrence of rupture, and the dimensions of the lesion were also observed, focusing in smaller aneurysms (<5 mm) and their powerful bleeding.

Aneurysms were arbitrarily classified according to its largest diameter: small (<5 mm), medium (5–10 mm), large (11–25 mm), and giant (>25 mm).[3] In cases with more than one aneurysm, only the treatment with clipped lesion was considered.

Clinical patients’ status at the time of discharge was evaluated with the modified Rankin scale (mRS) to characterize the related morbidity.

A Medline literature search in the past 5 years was performed using the terms: “an intracranial aneurysm,” “small cerebral aneurysm,” “cerebral hemorrhage,” “subarachnoid hemorrhage,” and “an aneurysm clipped.” We collected 357 papers from the literature search from which we selected 50 that were focused on our research. Articles published before the period of the search were eventually consulted given to its relevance to our discussion.

Results

During the 15-month period of the study, 125 patients underwent surgery for the treatment of cerebral aneurysms. Seven patients were due to incomplete information in the medical files.

Among the 118 patients considered for analysis, 31 (26.3%) were male and 87 (73.7%) female. The average age was 54.1 years, with a mean deviation of 8.07, ranging between 28 and 86 years. Ruptured aneurysms were prevalent in 61 patients (51.6%) and according to the Hunt-Hess scale were classified as Grade 1 (3 cases), Grade 2 (30 cases), Grade 3 (12 cases), Grade 4 (8 cases), and Grade 5 (6 cases).

The majority of the aneurysms were located in the middle cerebral artery (MCA; 51 cases, 43.2%; 25 ruptured and 26 unruptured), in the posterior communicating artery (23 cases, 19.4%; 13 ruptured and 10 unruptured), and in the anterior communicating artery (18 cases, 15.2%; 14 ruptured and 4 unruptured) showing in Table 1. In the small aneurysm group, the most common site of the lesion was MCA (15 cases, 60%; 5 ruptured and 10 unruptured) and Acoma (5 cases, 20%; all ruptured), representing in Table 1.

Table 1.

Distribution by the topography of ruptured and unruptured aneurysms (all cases)

Topography Ruptured Unruptured
ACoA 14 4
ACA 1 1
MCA 25 26
Pericalosa 1 1
ICA 2 4
PCoA 13 10
OPHT 1 8
CH 0 0
HIPOPH 1 1
CPA 2 0
Basilar 1 1
Vertebral 0 1

ACoA – Anterior communicating artery; ACA – Anterior cerebral artery; MCA – Middle cerebral artery; PCoA – Posterior communicating artery; OPHT – Ophthalmic artery; HIPOPH – Superior hypophysial artery; CPA – Cerebral posterior artery; ICA – Internal carotid artery

Among the patients with small unruptured aneurysms submitted to surgery, all (13/13) evolved with mild symptoms, remaining functional and independent for most daily activities (mRS-0, mRS-1, and mRS-2). Considering the 12 cases of aneurysms with <5 mm in diameter, two of these patients (16.6%) died – mRS-6. Three (25%) evolved with severe disability, restricted to bed, dependent on nursing care – mRS-5 [Table 2].

Table 2.

Distribution by the topography of ruptured and unruptured (aneurysms <5 mm)

Topography Ruptured Unruptured
ACoA 5 -
ACA - 1
MCA 5 10
Pericalosa 1 -
ICA - -
PCoA - 1
OPHT 1 -
CH - -
HIPOPH - 1
CPA - -
Basilar - -
Vertebral - -

ACoA – Anterior communicating artery; ACA – Anterior cerebral artery; MCA – Middle cerebral artery; PCoA – Posterior communicating artery; OPHT – Ophthalmic artery; HIPOPH – Superior hypophysial artery; CPA – Cerebral posterior artery; ICA – Internal carotid artery

According to the size, the aneurysms were classified as small (25 cases, 21%), medium (61 cases, 52%), large (28 cases, 24%), and giant (4 cases, 3%). The bleeding rate for the aneurysms of small size was 48%, 57% for the medium size, 46% for the large, and 25% for the giant aneurysms.

Among the risk factors, high blood pressure was found in 14 patients (56%) with small aneurysms (6 in the ruptured group and 8 in the unruptured), dyslipidemia in 6 patients (24%), smoking in 3 (12%), and diabetes mellitus in 2 (8%). The mean age of the patients with small aneurysms was 50.32 ± 11.48 years.

Stratifying the patients with smaller than five aneurysms in three subgroups, namely: I (5–4.1 mm), 7 cases; II (4–2.1 mm), 15 cases; and III (≤2 mm), 3 cases, we observed a prevalence of rupture of 42.8% (3/7) in the first, 40% (6/15) in the second, and 100% (3/3) in the third subgroup, with a respective mean age of 51.1 ± 12.4, 51.8 ± 9.8, and 40.7 ± 17 years. In addition, the prevalence of hypertension in these groups was 71.4% (5/7), 53.3% (8/15), 13.3% (2/15), and 0%, respectively. There was a trend to increased morbidity in subgroup II and III [Table 3].

Table 3.

Morbidity on discharge for patients with small aneurysms and in each subgroup of small aneurysms

Rankin 5-4.1 mm 4-2.1 mm ≤2 mm Ruptured Unruptured
0 - 1 1 2 3
1 2 1 - 3 9
2 - - - - 1
3 1 - - 1 -
4 - - 4 1 -
5 - 2 - 3 -
6 - 1 6 2 -

Discussion

SAH has a mortality rate of 40%–50%, and approximately 20% of the survivals present significant neurologic disability.[10,11] There is a consensus toward an early treatment of ruptured aneurysms. On the other hand, the recommendations regarding unruptured intracranial aneurysm management are still controversial.[12]

Aneurysm treatment complication should be considered in this context. Regarding embolization, the risks are aneurysm perforation, mechanical vasospasm, thromboembolism, and coil migration. Adverse events associated with surgery include infection, epidural or subdural hematomas, cranial nerve palsies, and ischemic infarction after clipping.[13,14,15,16,17] In a review of the subject, in 2013[18,19,20] found that an average rate of complications associated with clipping was 11%, ranging from 6.6% to 50%. Embolization analyses: the mean complication rate was 9%, between 4.1% and 28.6%.

A strong correlation between the aneurysm size aneurysm and the bled risk was pointed out by some authors[5,15,21,22,23,24,25,26,27,28,29,30,31,32,33,34] for whom the conservative treatment for aneurysms with <10 mm in diameter should be the recommendation. However, many published series demonstrated that small aneurysms (<10 mm) could bleed and should be operated.[3,6,8,9,13,14,15,16,17,18,19,25,26,27,35] This different point, they mean that the aneurysm diameter alone is not an accurate predictor for the risk of rupture.[20] Risk factors such as high blood pressure, young age, posterior circulation localization, and family history of SAH certainly contribute for aneurysm rupture.[22,29]

In our casuistic, aneurysms of all sizes presented SAH. The small number of patients with giant aneurysms (4 patients), the absence of a follow-up (retrospective analysis), selection bias, and the lack of control of some risk factors may be a possible mechanism. Among our cases, 48% (12/25) of aneurysms smaller than 5 mm ruptured, a bleeding tendency higher than the previously published.[3,5,10,15] This trend was confirmed when we stratified the group of small aneurysms in subgroups, noting that the prevalence of bleeding in small aneurysms remained high even in the subgroups below 2 mm, with a tendency to poor functional outcome after rupture of these smaller aneurysms.[36,37,38,39,40,41,42,43,44]

Besides, some authors suggest that small aneurysms are associated with more extensive SAH.[45] Taylor et al.[46] reported that aneurysms <5 mm tend to a more significant association with a higher score on the Fisher scale, although there was no difference in the incidence of vasospasm or overall outcomes.

In a review of 100 cases of patients with SAH reported an inverse relationship between the size of an aneurysm and the volume of cisternal blood.[46] Besides, some authors concluded that there is a higher risk of rupture during embolization of aneurysms smaller than 5 mm.[8,47,48]

The reason for this fact presented in our casuistic is unclear, and prospective studies are necessary to explain this inverse relationship between the size and the volume of blood. For large aneurysms (>10 mm), the reported bled risk was significantly higher, reaching 33.5% at 5 years and 55.9% at 10 years.[27] In our retrospective analysis, the rate of bleeding for these aneurysms was 44% and 52% for aneurysms more significant than 10 and 5 mm, respectively.

Some of the risk factors of aneurismal rupture (high blood pressure, diabetes mellitus, dyslipidemia, and smoking) were presented in our patients with small aneurysms, but there was no significant difference when comparing ruptured and unruptured lesions.

An aspect that was not considered in our study is the tendency to the aneurysm growth, and its implications on the aneurysm bled risk. In 2013[38] following 319 small untreated aneurysms (<7 mm), with a mean follow-up of 29.2 ± 20.6 months, observed an increase in size in 42 of these, 5 of which over 7 mm. Another interesting point to discuss is the decrease in the size of an aneurysm after its rupture, as described by some authors.[38,39] Taking this into account, the aneurysms considered to be small after rupture, could have their previous rupture risk underestimated by only analysing the size. Thus, retrospective analysis, such as ours, may overestimate the rates of bleeding for small aneurysms.

This study suggests that small aneurysms represent a significant number of the ruptured lesions (20%, 2/61), leading us to postulate that the standard aneurysm treatment has to be considered.

Limitations of the study

This is a retrospective study, and all inherent method limitations do apply. The limited sample, losses of data registration, and its heterogeneity are potential flaws. We also did not have a sufficiently large number of cases; however, we can only affirm that we also have to consider surgery in a small aneurysm because they even can bleed and we deal with SAH.

Conclusion

Our data showed that aneurysms smaller than 5 mm (small) account for a significant portion of all aneurysms diagnosed, incidentally or not, with a considerable rupture rate. There was a trend to increased morbidity in subgroup < 4 mm. Consequently, our tendency nowadays is for the surgical treatment of these lesions, especially when it is associated with risk factors, such as hypertension and smoking, which are present. Further prospective studies with longer follow-up and larger samples are needed to strengthen these conclusions.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Acknowledgment

We would like to thank Professors Dr. Manoel Jacobsen Teixeira and Eberval Gadelha Figueiredo for their encouragement and dedication to their students.

References

  • 1.Chason JL, Hindman WM. Berry aneurysms of the circle of Willis; results of a planned autopsy study. Neurology. 1958;8:41–4. doi: 10.1212/wnl.8.1.41. [DOI] [PubMed] [Google Scholar]
  • 2.Inagawa T, Hirano A. Autopsy study of unruptured incidental intracranial aneurysms. Surg Neurol. 1990;34:361–5. doi: 10.1016/0090-3019(90)90237-j. [DOI] [PubMed] [Google Scholar]
  • 3.Ishibashi T, Murayama Y, Urashima M, Saguchi T, Ebara M, Arakawa H, et al. Unruptured intracranial aneurysms: Incidence of rupture and risk factors. Stroke. 2009;40:313–6. doi: 10.1161/STROKEAHA.108.521674. [DOI] [PubMed] [Google Scholar]
  • 4.Iwamoto H, Kiyohara Y, Fujishima M, Kato I, Nakayama K, Sueishi K, et al. Prevalence of intracranial saccular aneurysms in a Japanese community based on a consecutive autopsy series during a 30-year observation period. The Hisayama study. Stroke. 1999;30:1390–5. doi: 10.1161/01.str.30.7.1390. [DOI] [PubMed] [Google Scholar]
  • 5.Wiebers DO, Whisnant JP, Huston J, 3rd, Meissner I, Brown RD, Jr, Piepgras DG. Unruptured intracranial aneurysms: Natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362:103–10. doi: 10.1016/s0140-6736(03)13860-3. [DOI] [PubMed] [Google Scholar]
  • 6.Forget TR, Jr, Benitez R, Veznedaroglu E, Sharan A, Mitchell W, Silva M, et al. Areview of size and location of ruptured intracranial aneurysms. Neurosurgery. 2001;49:1322–5. doi: 10.1097/00006123-200112000-00006. [DOI] [PubMed] [Google Scholar]
  • 7.Guglielmi G, Viñuela F, Dion J, Duckwiler G. Electrothrombosis of saccular aneurysms via endovascular approach. Part 2: Preliminary clinical experience. J Neurosurg. 1991;75:8–14. doi: 10.3171/jns.1991.75.1.0008. [DOI] [PubMed] [Google Scholar]
  • 8.Russell SM, Lin K, Hahn SA, Jafar JJ. Smaller cerebral aneurysms producing more extensive subarachnoid hemorrhage following rupture: A radiological investigation and discussion of theoretical determinants. J Neurosurg. 2003;99:248–53. doi: 10.3171/jns.2003.99.2.0248. [DOI] [PubMed] [Google Scholar]
  • 9.Roos EJ, Rinkel GJ, Velthuis BK, Algra A. The relation between aneurysm size and outcome in patients with subarachnoid hemorrhage. Neurology. 2000;54:2334–6. doi: 10.1212/wnl.54.12.2334. [DOI] [PubMed] [Google Scholar]
  • 10.Fogelholm R, Hernesniemi J, Vapalahti M. Impact of early surgery on outcome after aneurysmal subarachnoid hemorrhage. A population-based study. Stroke. 1993;24:1649–54. doi: 10.1161/01.str.24.11.1649. [DOI] [PubMed] [Google Scholar]
  • 11.van Gijn J, Rinkel GJ. Subarachnoid haemorrhage: Diagnosis, causes and management. Brain. 2001;124:249–78. doi: 10.1093/brain/124.2.249. [DOI] [PubMed] [Google Scholar]
  • 12.Maslehaty H, Ngando H, Meila D, Brassel F, Scholz M, Petridis AK, et al. Estimated low risk of rupture of small-sized unruptured intracranial aneurysms (UIAs) in relation to intracranial aneurysms in patients with subarachnoid haemorrhage. Acta Neurochir (Wien) 2013;155:1095–100. doi: 10.1007/s00701-013-1688-y. [DOI] [PubMed] [Google Scholar]
  • 13.Salary M, Quigley MR, Wilberger JE., Jr Relation among aneurysm size, amount of subarachnoid blood, and clinical outcome. J Neurosurg. 2007;107:13–7. doi: 10.3171/JNS-07/07/0013. [DOI] [PubMed] [Google Scholar]
  • 14.Weir B, Disney L, Karrison T. Sizes of ruptured and unruptured aneurysms in relation to their sites and the ages of patients. J Neurosurg. 2002;96:64–70. doi: 10.3171/jns.2002.96.1.0064. [DOI] [PubMed] [Google Scholar]
  • 15.Sonobe M, Yamazaki T, Yonekura M, Kikuchi H. Small unruptured intracranial aneurysm verification study: SUAVe study, Japan. Stroke. 2010;41:1969–77. doi: 10.1161/STROKEAHA.110.585059. [DOI] [PubMed] [Google Scholar]
  • 16.Juvela S, Porras M, Heiskanen O. Natural history of unruptured intracranial aneurysms: A long-term follow-up study. J Neurosurg. 1993;79:174–82. doi: 10.3171/jns.1993.79.2.0174. [DOI] [PubMed] [Google Scholar]
  • 17.Beck J, Rohde S, Berkefeld J, Seifert V, Raabe A. Size and location of ruptured and unruptured intracranial aneurysms measured by 3-dimensional rotational angiography. Surg Neurol. 2006;65:18–25. doi: 10.1016/j.surneu.2005.05.019. [DOI] [PubMed] [Google Scholar]
  • 18.Juvela S, Porras M, Poussa K. Natural history of unruptured intracranial aneurysms: Probability of and risk factors for aneurysm rupture. J Neurosurg. 2008;108:1052–60. doi: 10.3171/JNS/2008/108/5/1052. [DOI] [PubMed] [Google Scholar]
  • 19.Ohashi Y, Horikoshi T, Sugita M, Yagishita T, Nukui H. Size of cerebral aneurysms and related factors in patients with subarachnoid hemorrhage. Surg Neurol. 2004;61:239–45. doi: 10.1016/S0090-3019(03)00427-0. [DOI] [PubMed] [Google Scholar]
  • 20.Kashiwazaki D, Kuroda S Sapporo SAH Study Group. Size ratio can highly predict rupture risk in intracranial small (<5 mm) aneurysms. Stroke. 2013;44:2169–73. doi: 10.1161/STROKEAHA.113.001138. [DOI] [PubMed] [Google Scholar]
  • 21.Dhar S, Tremmel M, Mocco J, Kim M, Yamamoto J, Siddiqui AH, et al. Morphology parameters for intracranial aneurysm rupture risk assessment. Neurosurgery. 2008;63:185–96. doi: 10.1227/01.NEU.0000316847.64140.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Nahed BV, DiLuna ML, Morgan T, Ocal E, Hawkins AA, Ozduman K, et al. Hypertension, age, and location predict rupture of small intracranial aneurysms. Neurosurgery. 2005;57:676–83. [PubMed] [Google Scholar]
  • 23.Hamada J, Morioka M, Yano S, Kai Y, Ushio Y. Incidence and early prognosis of aneurysmal subarachnoid hemorrhage in Kumamoto Prefecture, Japan. Neurosurgery. 2004;54:31–7. doi: 10.1227/01.neu.0000097196.55204.0b. [DOI] [PubMed] [Google Scholar]
  • 24.International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms – Risk of rupture and risks of surgical intervention. N Engl J Med. 1998;339:1725–33. doi: 10.1056/NEJM199812103392401. [DOI] [PubMed] [Google Scholar]
  • 25.Juvela S. Prevalence of and risk factors for intracranial aneurysms. Lancet Neurol. 2011;10:595–7. doi: 10.1016/S1474-4422(11)70125-9. [DOI] [PubMed] [Google Scholar]
  • 26.Juvela S, Porras M, Poussa K. Natural history of unruptured intracranial aneurysms: Probability of and risk factors for aneurysm rupture. J Neurosurg. 2000;93:379–87. doi: 10.3171/jns.2000.93.3.0379. [DOI] [PubMed] [Google Scholar]
  • 27.Tsutsumi K, Ueki K, Morita A, Kirino T. Risk of rupture from incidental cerebral aneurysms. J Neurosurg. 2000;93:550–3. doi: 10.3171/jns.2000.93.4.0550. [DOI] [PubMed] [Google Scholar]
  • 28.Raymond J, Guillemin F, Proust F, Molyneux AJ, Fox AJ, Claiborne JS, et al. Unruptured intracranial aneurysms. A Critical review of the international study of unruptured intracranial aneurysms (ISUIA) and of appropriate methods to address the clinical problem. Interv Neuroradiol. 2008;14:85–96. doi: 10.1177/159101990801400111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Bederson JB, Awad IA, Wiebers DO, Piepgras D, Haley EC, Jr, Brott T, et al. Recommendations for the management of patients with unruptured intracranial aneurysms: A Statement for healthcare professionals from the stroke council of the American Heart Association. Stroke. 2000;31:2742–50. doi: 10.1161/01.str.31.11.2742. [DOI] [PubMed] [Google Scholar]
  • 30.Komotar RJ, Mocco J, Solomon RA. Guidelines for the surgical treatment of unruptured intracranial aneurysms: The first annual J. Lawrence pool memorial research symposium – Controversies in the management of cerebral aneurysms. Neurosurgery. 2008;62:183–93. doi: 10.1227/01.NEU.0000311076.64109.2E. [DOI] [PubMed] [Google Scholar]
  • 31.Güresir E, Vatter H, Schuss P, Platz J, Konczalla J, de Rochement Rdu M, et al. Natural history of small unruptured anterior circulation aneurysms: A prospective cohort study. Stroke. 2013;44:3027–31. doi: 10.1161/STROKEAHA.113.001107. [DOI] [PubMed] [Google Scholar]
  • 32.Kemp WJ, 3rd, Fulkerson DH, Payner TD, Leipzig TJ, Horner TG, Palmer EL, et al. Risk of hemorrhage from de novo cerebral aneurysms. J Neurosurg. 2013;118:58–62. doi: 10.3171/2012.9.JNS111512. [DOI] [PubMed] [Google Scholar]
  • 33.Raabe A, Seifert V, Schmiedek P, Steinmetz H, Bertalanffy H, Steiger HJ, et al. Recommendations for the management of unruptured intracranial aneurysms. Zentralbl Neurochir. 2002;63:70–6. doi: 10.1055/s-2002-33972. [DOI] [PubMed] [Google Scholar]
  • 34.Wermer MJ, van der Schaaf IC, Algra A, Rinkel GJ. Risk of rupture of unruptured intracranial aneurysms in relation to patient and aneurysm characteristics: An updated meta-analysis. Stroke. 2007;38:1404–10. doi: 10.1161/01.STR.0000260955.51401.cd. [DOI] [PubMed] [Google Scholar]
  • 35.Sato K, Yoshimoto Y. Risk profile of intracranial aneurysms: Rupture rate is not constant after formation. Stroke. 2011;42:3376–81. doi: 10.1161/STROKEAHA.111.625871. [DOI] [PubMed] [Google Scholar]
  • 36.Kalani MY, Zabramski JM, Kim LJ, Chowdhry SA, Mendes GA, Nakaji P, et al. Long-term follow-up of blister aneurysms of the internal carotid artery. Neurosurgery. 2013;73:1026–33. doi: 10.1227/NEU.0000000000000147. [DOI] [PubMed] [Google Scholar]
  • 37.Signorelli F, Scholtes F, Bojanowski MW. Very small intracranial aneurysms: Clip or coil. Neurochirurgie. 2012;58:156–9. doi: 10.1016/j.neuchi.2012.03.004. [DOI] [PubMed] [Google Scholar]
  • 38.Chien A, Liang F, Sayre J, Salamon N, Villablanca P, Viñuela F, et al. Enlargement of small, asymptomatic, unruptured intracranial aneurysms in patients with no history of subarachnoid hemorrhage: The different factors related to the growth of single and multiple aneurysms. J Neurosurg. 2013;119:190–7. doi: 10.3171/2013.3.JNS121469. [DOI] [PubMed] [Google Scholar]
  • 39.Chien A, Sayre J, Viñuela F. Comparative morphological analysis of the geometry of ruptured and unruptured aneurysms. Neurosurgery. 2011;69:349–56. doi: 10.1227/NEU.0b013e31821661c3. [DOI] [PubMed] [Google Scholar]
  • 40.Matsubara S, Hadeishi H, Suzuki A, Yasui N, Nishimura H. Incidence and risk factors for the growth of unruptured cerebral aneurysms: Observation using serial computerized tomography angiography. J Neurosurg. 2004;101:908–14. doi: 10.3171/jns.2004.101.6.0908. [DOI] [PubMed] [Google Scholar]
  • 41.Ohman J, Heiskanen O. Timing of operation for ruptured supratentorial aneurysms: A prospective randomized study. J Neurosurg. 1989;70:55–60. doi: 10.3171/jns.1989.70.1.0055. [DOI] [PubMed] [Google Scholar]
  • 42.Whitfield PC, Kirkpatrick PJ. Timing of surgery for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev. 2001;2:CD001697. doi: 10.1002/14651858.CD001697. [DOI] [PubMed] [Google Scholar]
  • 43.Kassell NF, Torner JC, Haley EC, Jr, Jane JA, Adams HP, Kongable GL. The international cooperative study on the timing of aneurysm surgery. Part 1: Overall management results. J Neurosurg. 1990;73:18–36. doi: 10.3171/jns.1990.73.1.0018. [DOI] [PubMed] [Google Scholar]
  • 44.Li H, Pan R, Wang H, Rong X, Yin Z, Milgrom DP, et al. Clipping versus coiling for ruptured intracranial aneurysms: A systematic review and meta-analysis. Stroke. 2013;44:29–37. doi: 10.1161/STROKEAHA.112.663559. [DOI] [PubMed] [Google Scholar]
  • 45.Fraser JF, Riina H, Mitra N, Gobin YP, Simon AS, Stieg PE, et al. Treatment of ruptured intracranial aneurysms: Looking to the past to register the future. Neurosurgery. 2006;59:1157–66. doi: 10.1227/01.NEU.0000245623.70344.F7. [DOI] [PubMed] [Google Scholar]
  • 46.Taylor CL, Steele D, Kopitnik TA, Jr, Samson DS, Purdy PD. Outcome after subarachnoid hemorrhage from a very small aneurysm: A case-control series. J Neurosurg. 2004;100:623–5. doi: 10.3171/jns.2004.100.4.0623. [DOI] [PubMed] [Google Scholar]
  • 47.Sluzewski M, Bosch JA, van Rooij WJ, Nijssen PC, Wijnalda D. Rupture of intracranial aneurysms during treatment with Guglielmi detachable coils: Incidence, outcome, and risk factors. J Neurosurg. 2001;94:238–40. doi: 10.3171/jns.2001.94.2.0238. [DOI] [PubMed] [Google Scholar]
  • 48.van Rooij WJ, Sluzewski M, Beute GN, Nijssen PC. Procedural complications of coiling of ruptured intracranial aneurysms: Incidence and risk factors in a consecutive series of 681 patients. AJNR Am J Neuroradiol. 2006;27:1498–501. [PMC free article] [PubMed] [Google Scholar]

Articles from Asian Journal of Neurosurgery are provided here courtesy of Thieme Medical Publishers

RESOURCES